Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides According to Mode of Action1

PI-94

Frederick M. Fishel2

This guide addresses resistance to pesticides and large populations with a rapid rate of reproduction. describes the Fungicide Resistance Action Weeds were the last category of pests to show Committee's (FRAC) classification of fungicides and resistance because they only reproduce, at most, once bactericides registered for use in Florida by their per year. By contrast, insects reproduce with multiple modes of action. A cross reference of common names generations in a single year, and some bacteria and for active ingredients -- with corresponding examples fungi reproduce several times in a single hour. of their trade names -- is also provided. Where large populations exist, great genetic Fungicide-resistant plant pathogens are not new. diversity exists within the population. Within these Although the first confirmation of fungicide large populations, there will be several individuals resistance was in 1960, there were few subsequent that are tolerant of chemical-control measures, incidences up until 1970. Since then, there have been perhaps only one in a million or billion. Pests more incidences, especially with the introduction of typically become resistant when the same pesticide is systemic fungicides. Also of concern has been the used repeatedly within a single year or for several shortening amount of time taken for resistance to consecutive years. Some researchers believe selection emerge, sometimes within two years of a new pressure forces pests to mutate. However, there are commercial fungicide introduction. more likely reasons for resistance:

Fungicide resistance is not unique to plant ¥ There were always a few of the resistant types pathogens. Insecticide-resistant insects, present. herbicide-resistant weeds and antibiotic-resistant bacteria are well documented. These resistant pests ¥ When the pesticide is applied, the susceptible have two common traits: they have exceptionally types are controlled, and then the smaller, resistant populations increase and re-infest the site.

1. This document is PI-94, one of a series of the Pesticide Information Office, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Original publication date, February 2006. Revised January 2009. Visit the EDIS Web site at http://edis.ifas.ufl.edu. 2. Frederick M. Fishel, associate professor, Agronomy Department, and director, Pesticide Information Office; Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611. The use of trade names in this publication is solely for the purpose of providing specific information. UF/IFAS does not guarantee or warranty the products named, and references to them in this publication does not signify our approval to the exclusion of other products of suitable composition.

The Institute of Food and Agricultural Sciences (IFAS) is an Equal Opportunity Institution authorized to provide research, educational information and other services only to individuals and institutions that function with non-discrimination with respect to race, creed, color, religion, age, disability, sex, sexual orientation, marital status, national origin, political opinions or affiliations. U.S. Department of Agriculture, Cooperative Extension Service, University of Florida, IFAS, Florida A. & M. University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Interim Dean Millie Ferrer.

Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 2

Cross Resistance Versus Multiple ¥ Cross resistance with existing fungicides; Resistance ¥ Laboratory studies have shown resistant More than 50 different fungicide active mutants within the population; ingredients and many more trade products, including ¥ The active ingredient is known for the practice mixtures, are available to agricultural producers in of repetitive use or sustained treatments; Florida today. Many of these active ingredients work in the same way; in other words, they have the same ¥ The active ingredient is known to have an mode of action. extensive area of use; and,

Although there are numerous trade products ¥ The target plant pathogens are known to have available, there are fewer than 20 growth mechanisms large populations with rapid multiplication. affected by these fungicides. When a certain plant pathogen is not controlled by fungicides affecting the The system is encouraged by FRAC for same growth process, it is said to be cross-resistant. fungicide registrants to indicate the mode-of-action An example of a plant pathogen that has cross group in a uniform location on their product labels resistance is one that is resistant to fungicides in the Some registrants identify the mode-of-action group chemical groups, triazoles and pyrimidines, both on the front panel of their product labels. which are demethylation inhibitors which disrupt Similar systems have been proposed and sterol synthesis. encouraged for herbicides and insecticides. A more serious concern is multiple resistance. Because of the great variety of trade names and This phenomenon occurs when a plant pathogen is package mixtures of fungicides, it is difficult for not controlled by fungicides that affect different plant-growth processes. For example, a plant agricultural producers to keep track of which modes of action they use. pathogen that is resistant to fungicides that inhibit both mitosis and protein synthesis, two differing Additional Information fungal growth processes, would be labeled as a plant pathogen having multiple resistance. Fungicide Resistance Action Committee (FRAC): http://www.frac.info/ Fungicide Selection McCoy, C.W., M.E. Rogers, and L.W. Timmer. Farmers and crop advisors need to know which 2004. 2005 Florida citrus pest management guide: fungicides are best suited to combat resistant plant pesticide resistance and resistance management. pathogens. To support the use of fungicides suitable UF/IFAS EDIS Document ENY-624. for resistance management, the FRAC numerical http://edis.ifas.ufl.edu/CG026. classification of fungicides in Table 1 is used by some manufacturers on their fungicide labels. The Tomlin, C.D.S., ed. 2003. The pesticide manual: fungicides are classified according to their modes of a world compendium, 13th edition. The British Crop action, collective and chemical group names, and Protection Council. 1250 pp., ISBN 1 901396 13 4. active ingredient common names. Some examples of popular trade names are provided in Table 2 as a cross reference.

The tables do not include all fungicides that are registered for use globally or in the U.S.; rather, only those available in Florida. Those which have an intrinsic “high risk” of resistance evolution are identified. “High risk” is determined by the following indicators: Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 3

Table 1. FRAC's classification of fungicides registered for use in Florida by FRAC numerical code, mode of action, chemical group, and active-ingredient common name with resistance risk indication.

FRAC Mode of action Group name Chemical group Common code* name/resistance risk 4 Nucleic acids PhenylAmides Acylalanines Metalaxyl synthesis Metalaxyl-M (Mefenoxam)

HIGH RISK 32 Heteroaromatics Isothiazolones Octhilinone RESISTANCE NOT KNOWN 1 Mitosis and cell MBC Ð Fungicides Benzimidazoles Carbendazim division (Methyl Thiabendazole Benzimidazole HIGH RISK Carbamates) Thiophanates Thiophanate-methyl HIGH RISK 22 Benzamides Toluamides Zoxamide LOW TO MEDIUM RISK 43 Pyridinylmethyl- Fluopicolide benzamides RESISTANCE NOT KNOWN 7 Respiration Carboxamides Phenylbenzamides Flutolanil MEDIUM RISK Oxathiincarboxamides Carboxin Oxycarboxin MEDIUM RISK Pyridinecarboxamides Boscalid MEDIUM RISK 11 QoI Ð fungicides Methoxy acrylates Azoxystrobin (Quinone outside HIGH RISK Inhibitors) Methoxy carbamates Pyraclostrobin HIGH RISK Oximinoacetates Kresoxim-methyl Trifloxystrobin HIGH RISK Oxazolidinediones Famoxadone HIGH RISK Dihydrodioxazines Fluoxastrobin HIGH RISK Imidazolinones Fenamidone HIGH RISK 29 Uncouplers of 2,6-dinitrophenyl crotonates Fluazinam oxidative LOW RISK phosphorylation 30 Organo tin Tri phenyl tin compounds Fentin hydroxide compounds LOW TO MEDIUM RISK Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 4

Table 1, continued. FRAC's classification of fungicides registered for use in Florida by FRAC numerical code, mode of action, chemical group, and active-ingredient common name with resistancerisk indication.

9 Amino acids and AP Ð fungicides Anilino-pyrimidines Cyprodinil protein synthesis (Anilino-Pyrimidines) Pyrimethanil MEDIUM RISK 25 Glucopyranosyl Glucopyranosyl antibiotic Streptomycin antibiotic HIGH RISK 41 Tetracycline antibiotic Tetracycline antibiotic Oxytetracycline HIGH RISK 13 Signal transduction Quinolines Quinolines Quinoxyfen MEDIUM RISK 12 PP-fungicides Phenylpyrroles Fludioxonil (PhenylPyrroles) LOW TO MEDIUM RISK 2 Dicarboximides Dicarboximides Iprodione Vinclozolin MEDIUM TO HIGH RISK 14 Lipids and AH-fungicides Aromatic hydrocarbons Chloroneb membrane (Aromatic Dicloran synthesis Hydrocarbons) Quintozene (PCNB) LOW TO MEDIUM RISK Heteroaromatics 1,2,4-thiadiazoles Etridiazole LOW TO MEDIUM RISK 28 Carbamates Carbamates Propamocarb

LOW TO MEDIUM RISK 40 CAA-fungicides Cinnamic acid amides Dimethomorph (Carboxylic Acid LOW TO MEDIUM Amides) RISK Mandelic acid amides Mandipropamid LOW TO MEDIUM RISK Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 5

3 Sterol biosynthesis DMI-fungicides Piperazines Triforine in membranes (DeMethylation MEDIUM RISK Inhibitors) Pyrimidines Fenarimol MEDIUM RISK Imidazoles Imazalil Triflumizole

MEDIUM RISK Triazoles Difenoconazole Fenbuconazole Ipconazole Metconazole Myclobutanil Propiconazole Prothioconazole Tebuconazole Tetraconazole Triadimefon Triadimenol MEDIUM RISK 5 Amines (Morpholines) Piperidines Piperalin LOW TO MEDIUM RISK 17 Hydroxyanilides Hydroxyanilides Fenhexamid LOW TO MEDIUM RISK 19 Glucan synthesis Polyoxins Peptidyl pyrimidine Polyoxin nucleoside MEDIUM RISK P Host plant defense Benzo-thiodiazole Benzo-thiadiazole Acibenzolar-S-methyl induction RESISTANCE NOT KNOWN 27 Unknown mode of Cyanoacetamide- Cyanoacetamide-oxime Cymoxanil action oxime LOW TO MEDIUM RISK 33 Phosphonates Ethyl phosphonates Fosetyl-Al Phosphorous acid and salts LOW RISK NC Diverse Diverse Mineral oils Organic oils Potassium bicarbonate Material of biological origin RESISTANCE NOT KNOWN Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 6

M1 Multi-site contact Inorganic Inorganic Copper (different activity salts) LOW RISK M2 Sulfur LOW RISK M3 Dithiocarbamates Dithiocarbamates and Ferbam and relatives relatives Mancozeb Maneb Metiram Thiram Ziram LOW RISK M4 Phthalimides Phthalimides Captan Folpet LOW RISK M5 Chloronitriles Chloronitriles Chlorothalonil LOW RISK M7 Guanidines Guanidines Dodine Resistance reported in Venturia inaequalis suggesting that dodine may not be a multi-site inhibitor. Resistance management recommended *Numbers and letters are used to distinguish the fungicide groups. The numbers were assigned primarily according to the time of product introduction to the market. The letter abbreviations are as follows: P = host plant defense inducers; M = multi-site contact activity; and NC = not classified.

Table 2. Cross listing of active-ingredient common names with trade products registered for use in Florida.

Common name Trade products*¨ Acibenzolar-S-methyl Actigard, Blockade Azoxystrobin (HIGH RISK) Abound, Amistar, Azo-Shield, Azotech, Dynasty, Headway, Heritage, Highway, Quadris, Quilt, Seed Shield, Sporgard, Uniform Boscalid Endura, Pristine Captan Captan, Captec, Captevate, Enhance, Fungitrol, SA-50, TCI, Trilex, Vitavax PC Carbendazim (HIGH RISK) Fungiblock, Mauget, Mergal, Polyphase, Rocima, placeCityTroy Mergal, Troysan Carboxin Allerax, Cotgard, Enhance, Kernel Guard, Kickstart, Latitude, Prevail, Vitavax Chloroneb Catapult, Terraneb, Nu-Coat Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 7

Table 2, continued. Cross listing of active-ingredient common names with trade products registered for use in Florida.

Chlorothalonil Acticide PAX, Applause, Bravo, Busan, Chemnut, Chemtreat, Chloronil, Chlorostar, Chlorothalonil, Concorde, Countdown, Daconil, Densil, Disarm, Docket, Echo, Ensign, Equus, Flouronil, Fungitrol, Initiate, Instrata, Mainsail, Manicure, Maxide, Mold-Ram Nipcocide, Pegasus, Peregrine, Prominence, Quadris, Quali-Pro, Regal Consyst, Ridomil Gold, Rocima, SA-50, Sipcam, Spectro, Tee-1-Up, Thor, Tilt, TM + CTN Copper (carbonate) CMC, Micropro, Phibrowood, Sustain, UCU, Wolman E Copper (ethanolamine complex) Various swimming pool treatments Copper (ethylenediamine Current, Harpoon, Komeen, Pondmaster complex) Copper (hydroxide) Champ, Champion, Cu-Bor, Cupro, Funguran, GX-569, Junction, Kentan, Kocide, Kop-Hydroxide, Mankocide, Neptune, Nu-Cop, Ridomil Gold Copper, Spin Out, Copper (metallic) Various algaecides and anti-fouling paints Copper (naphthenate) Various wood preservatives Copper (oxychloride) placeCityAgra Cop, Badge, COC, Kocide COC Copper (salts of fatty and rosin Camelot, Tenn-Cop acids) Copper (sulfate pentahydrate) Various swimming pool treatments Copper (triethanolamine complex) Various algaecides and other water treatments Copper (I oxide) Various anti-fouling paints Copper (II oxide) Various wood preservatives Cymoxanil Curzate, Evolve, Tanos Cyprodinil Switch, Vangard Dicloran Botran Difenoconazole Cruiser, Dividend, Inspire, Revus, Seed Shield Dimethomorph Acrobat Dodine Elast, Syllit Famoxadone (HIGH RISK) Tanos Fenamidone (HIGH RISK) Reason Fenarimol Rubigan Fenbuconazole Enable, Indar Fenhexamid Captevate, Decree, Elevate, Fentin hydroxide Agri Tin, Enable, Orbit, Super Tin Ferbam Ferbam Fluazinam Omega Fludioxonil Apron, Cruiser, Dynasty, Fludi-Shield, Graduate, Hurricane, Instrata, Maxim, Medallion, Scholar, Seed Shield, Sporgard, Switch Fluoxastrobin (HIGH RISK) Evito Flutolanil Artisan, Contrast, Convoy, Moncoat, Moncut, Prostar, Sysstar Folpet Folpet, Fungitrol, several wood preservatives Fosetyl-Al Aliette, Autograph, Avalon, Flanker, Legion, Linebacker, Novasource, Prodigy Signature, Quali-Pro Imazalil Clinafarm, Deccozil, Freshgard, Fungaflor, Magnate, Pacrite Ipconazole Vortex Iprodione 26/36, 26GT, placeCityAndersons, Chipco, Dovetail, Iprodione, Lesco, Nevado, OHP, Primeraone, Quali-Pro, Raven, Rovral, Sextant, TM + IP Kresoxim-methyl (HIGH RISK) Cygnus, Sovran Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 8

Table 2, continued. Cross listing of active-ingredient common names with trade products registered for use in Florida.

Mancozeb Acrobat MZ, Clevis, Cuprofix MZ, Dithane, Evolve, Fore, Gaucho, Gavel, Junction, Mancozide, Manhandle, Manzate, Maxim, Moncoat, Nubark, Penncozeb, Pentathlon, Potato Seed Treater, Protect, Ridomil Gold MZ, SA-50, Stature, Tops MZ, Wingman, Zyban Maneb Maneb, Manex, Pentathlon Metalaxyl (HIGH RISK) Acquire, Allegiance, Allerax, Catapult, Cotgard, Latitude, Metastar, Prevail, Sebring, System 3, Trilex Metalaxyl-M (Mefenoxam) (HIGH Apron, Axle, Cruiser, Dividend, Dynasty, Fenox Flouronil, Hurricane, RISK) Mefenoxam, Ridomil Gold, Seed Shield, Subdue, Twist, Ultra Flourish, Uniform Metiram Polyram Myclobutanil Clevis, Dynasty, Eagle, Green Light, Greenview, Hoist, Immunox, CityLaredo, Manhandle, Nova, Rally, Schultz, placeCitySonoma Octhilinone Acticide, Arch, Bio/Tec 95, Cleanwood, Dobercide, Kathon, Mergal, Milbrex, Moldex, Rocima, Skane, Tex-Stat, Thor, Troysan Oxycarboxin Provax Oxytetracylince (HIGH RISK) Bacastat, Fireline, Flameout, OTC Phosphorous acid Magellan, Phostrol Piperalin Pipron Polyoxin Endorse, Veranda Propamocarb Banol, Previcur, Proplant, Stellar Propiconazole Alamo, Antiblu, Artisan, Banner, Bumper, Busan, Concert, Dorado, Fathom, Frameguard, Headway, Highway, Honor Guard, Instrata, Kestrel, Kop-Coat, Monterey, Mycostat, Orbit, Pack PT, Premier, Primeraone, Procon, Propensity, Propimax, Prosan, Quilt, Savvi, Spectator, Stratego, Tilt, Tranquilizer, Troysan, Wolman Pyraclostrobin (HIGH RISK) Cabrio, Coronet, Diamir, Headline, Insignia, Pageant, Pristine, Stamina, Twinline PCNB Blocker, Parflo, Prevail, System 3, Terraclor, Turfcide, Vitavax Pyrimethanil Penbotec, Scala Quinoxyfen Quintec Streptomycin (HIGH RISK) Agri Mycin, Bac-Master, Firewall, Streptrol Sulfur Many commercial products Thiabendazole (HIGH RISK) Add-2, Arbotect, Azotect, Decco Salt, Freshgard, Irgagard, Krud Kutter, Mertect, Metasol, Shield-Brite, Sporgard, Stay-Clean, Super Mildex, Tecto Thiophanate-methyl (HIGH RISK) 26/36, 3336, Allban, Banrot, Cavalier, Consyst, Dovetail, Evolve, Fungo, Infuse, OHP, Peregrine, Primeraone, Prominence, Quali-Pro, SA-50, Spectro, Sysstar, Systec, T-Bird, T-Methyl, Tee-1-Up, Tee-Off, TM, Tops, Topsin, Transom, T-Storm, Trilex Star Thiram 42-S, Allerax, Defiant, Raxil, Rootone, Spotrete, Protector L, Vitavax Triadimefon SA-50, Armada, Bayleton, Fung Away, Fung-Onil, Strike, Tartan, Turf Triadimenol Trilex Trifloxystrobin (HIGH RISK) Absolute, Adament, Armada, Compass, Distinguish, placeCityFlint, Gem, Stratego, Tartan, Trilex Triforine Orthenex, Rosepride Vinclozolin Curalan, Touche Ziram Vancide Zoxamide Gavel Fungicide Resistance Action Committee's (FRAC) Classification Scheme of Fungicides.... 9

Table 2, continued. Cross listing of active-ingredient common names with trade products registered for use in Florida.

*Trade product contains at least this sole active ingredient, but may be pre-mixed with additional active ingredients. Consult product label ingredient statements. ¨The use of trade names in this publication is solely for the purpose of providing specific information. UF/IFAS does not guarantee or warranty the products named, and references to them in this publication does not signify our approval to the exclusion of other products of suitable composition. Use pesticides safely. Read and follow directions on the manufacturer's label.